Mitochondrial DNA (mtDNA) has been the workhorse of research in phylogeography for almost two decades. However, concerns with basing evolutionary interpretations on mtDNA results alone have been voiced since the inception of such studies. Recently, some authors have suggested that the potential problems with mtDNA are so great that inferences about population structure and species limits are unwarranted unless corroborated by other evidence, usually in the form of nuclear gene data. Here we review the relative merits of mitochondrial and nuclear phylogeographical studies, using birds as an exemplar class of organisms. A review of population demographic and genetic theory indicates that mitochondrial and nuclear phylogeographical results ought to concur for both geographically unstructured populations and for populations that have long histories of isolation. However, a relatively common occurrence will be shallow, but geographically structured mtDNA trees-without nuclear gene corroboration-for populations with relatively shorter periods of isolation. This is expected because of the longer coalescence times of nuclear genes (approximately four times that of mtDNA); such cases do not contradict the mtDNA inference of recent isolation and evolutionary divergence. Rather, the nuclear markers are more lagging indicators of changes in population structure. A review of the recent literature on birds reveals the existence of relatively few cases in which nuclear markers contradict mitochondrial markers in a fashion not consistent with coalescent theory. Preliminary information from nuclear genes suggests that mtDNA patterns will prove to be robust indicators of patterns of population history and species limits. At equilibrium, mitochondrial loci are generally a more sensitive indicator of population structure than are nuclear loci, and mitochondrial estimates of F ST -like statistics are generally expected to exceed nuclear ones. Hence, invoking behavioural or ecological explanations of such differences is not parsimonious. Nuclear genes will prove important for quantitative estimates of the depths of haplotype trees, rates of population growth and values of gene flow.Keywords: Aves, coalescence, F-statistics, microsatellites, mtDNA, nuclear DNA Received 20 May 2007; revision received 5 February 2008; accepted 11 February 2008 IntroductionOur understanding of the evolutionary history of populations has been dramatically enhanced by the acquisition of molecular data that have revealed the distribution of genetic variation within and among populations. Surveys of allozyme variation were the method of choice in the period from the late 1960s to the mid-1980s (Avise 2000). However, well-documented limitations of allozymes resulted in their disuse when it became feasible to survey variation directly at the DNA level; after all, what could provide a better record of evolutionary history than the blueprint of heredity itself? Restriction enzyme digests of organelle DNA were used for a few years, but these soon were rep...
the contact area while avoiding steric clashes. Although VRC is d~stant from VRA and VRB withln an Fr-RBD monomer, VRC from one subunit is close to VRB of the adjacent subunit of the trlmer model, such that there are only three variable lobes per trirner, with each being composed of sequences from two Fr-RBD subunits (D. Fass, thesis, Massachusetts Institute
Subspecies are often used in ways that require their evolutionary independence, for example as proxies for units of conservation. Mitochondrial DNA sequence data reveal that 97% of continentally distributed avian subspecies lack the population genetic structure indicative of a distinct evolutionary unit. Subspecies considered threatened or endangered, some of which have been targets of expensive restoration efforts, also generally lack genetic distinctiveness. Although sequence data show that species include 1.9 historically significant units on average, these units are not reflected by current subspecies nomenclature. Yet, it is these unnamed units and not named subspecies that should play a major role in guiding conservation efforts and in identifying biological diversity. Thus, a massive reorganization of classifications is required so that the lowest ranks, be they species or subspecies, reflect evolutionary diversity. Until such reorganization is accomplished, the subspecies rank will continue to hinder progress in taxonomy, evolutionary studies and especially conservation.
Dispersal and vicariance are often contrasted as competing processes primarily responsible for spatial and temporal patterns of biotic diversity. Recent methods of biogeographical reconstruction recognize the potential of both processes, and the emerging question is about discovering their relative frequencies. Relatively few empirical studies, especially those employing molecular phylogenies that allow a temporal perspective, have attempted to estimate the relative roles of dispersal and vicariance. In this study, the frequencies of vicariance and dispersal were estimated in six lineages of birds that occur mostly in the aridlands of North America. Phylogenetic trees derived from mitochondrial DNA sequence data were compared for towhees (genus Pipilo), gnatcatchers (genus Polioptila), quail (genus Callipepla), warblers (genus Vermivora) and two groups of thrashers (genus Toxostoma). Di¡erent area cladograms were obtained depending on how widespread and missing taxa were coded. Nonetheless, no cladogram was obtained for which all lineages were congruent. Although vicariance was the dominant mode of evolution in these birds, approximately 25% of speciation events could have been derived from dispersal across a preexisting barrier. An expanded database is now needed to estimate the relative roles of each process. Applying a molecular clock calibration, nearly all speciation events are of the order of a million or more years old, much older than typically presumed.
Pleistocene glaciations have been suggested as major events influencing speciation rates in vertebrates. Avian paleontological studies suggest that most extant species evolved in the Pleistocene Epoch and that species' durations decreased through the Pleistocene because of heightened speciation rates. Molecular systematic studies provide another data base for testing these predictions. In particular, rates of diversification can be determined from molecular phylogenetic trees. For example, an increasing rate of speciation (but constant extinction) requires shorter intervals between successive speciation events on a phylogenetic tree. Examination of the cumulative distribution of reconstructed speciation events in mtDNA phylogenies of 11 avian genera, however, reveals longer intervals between successive speciation events as the present time is approached, suggesting a decrease in net diversification rate through the Pleistocene Epoch. Thus, molecular systematic studies do not indicate a pulse of Pleistocene diversification in passerine birds but suggest, instead, that diversification rates were lower in the Pleistocene than for the preceding period. Documented habitat shifts likely led to the decreased rate of diversification, although from molecular evidence we cannot discern whether speciation rates decreased or extinction rates increased.Temporal changes in rates of speciation and extinction result in variation in the net rate of organismal diversification through time (1). Documenting and explaining these rate changes represent major challenges in evolutionary biology. The Pleistocene Epoch presents such a challenge because of its marked environmental fluctuations and its recency, which permit detailed study of factors that influenced changes in species diversity. Many evolutionary biologists hypothesize accelerated vertebrate speciation in North America during the Pleistocene Epoch (2-5), owing to glacial advances and retreats that provided geographic barriers necessary for speciation (2, 3). Mayr (6) remarked, "Evolutionists agree on the overwhelming importance of Pleistocene barriers in the speciation of temperate zone animals." However, major Pleistocene extinctions are also known for some groups, including plants (7-9). The marked environmental effects of the Pleistocene Epoch clearly influenced rates of diversification, although the relative roles of speciation and extinction are unclear.The relatively high passerine bird diversity in modern fauna is often attributed to a burst of Pleistocene speciation (2, 3). Selander (2) also predicted that most extant bird species originated in the Pleistocene Epoch. A correlate of accelerated Pleistocene speciation concerns the average duration of bird species in the fossil record. Brodkorb (10) proposed that passerine bird species persisted for an average of three million yr in the Pliocene Epoch but only 500,000-1,000,000 yr in the Pleistocene Epoch. Thus, he predicted that species' durations decreased as the present time was approached. Although theseThe...
To assess the role of human disturbances in species' extinction requires an understanding of the species population history before human impact. The passenger pigeon was once the most abundant bird in the world, with a population size estimated at 3-5 billion in the 1800s; its abrupt extinction in 1914 raises the question of how such an abundant bird could have been driven to extinction in mere decades. Although human exploitation is often blamed, the role of natural population dynamics in the passenger pigeon's extinction remains unexplored. Applying high-throughput sequencing technologies to obtain sequences from most of the genome, we calculated that the passenger pigeon's effective population size throughout the last million years was persistently about 1/10,000 of the 1800's estimated number of individuals, a ratio 1,000-times lower than typically found. This result suggests that the passenger pigeon was not always super abundant but experienced dramatic population fluctuations, resembling those of an "outbreak" species. Ecological niche models supported inference of drastic changes in the extent of its breeding range over the last glacial-interglacial cycle. An estimate of acorn-based carrying capacity during the past 21,000 y showed great year-to-year variations. Based on our results, we hypothesize that ecological conditions that dramatically reduced population size under natural conditions could have interacted with human exploitation in causing the passenger pigeon's rapid demise. Our study illustrates that even species as abundant as the passenger pigeon can be vulnerable to human threats if they are subject to dramatic population fluctuations, and provides a new perspective on the greatest human-caused extinction in recorded history
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